Somatosensory and auditory convergence in the lateral nucleus of the amygdala.
Abstract
Previous studies have shown that the lateral nucleus of the amygdala (AL) is essential in auditory fear conditioning and that neurons in the AL respond to auditory stimuli. The goals of the present study were to determine whether neurons in the AL are also responsive to somatosensory stimuli and, if so, whether single neurons in the AL respond to both auditory and somatosensory stimulation. Single-unit activity was recorded in the AL in anesthetized rats during the presentation of acoustic (clicks) and somatosensory (footshock) stimuli. Neurons in the dorsal subdivision of the AL responded to both somatosensory and auditory stimuli, whereas neurons in the ventrolateral AL responded only to somatosensory stimuli and neurons in the ventromedial AL did not respond to either stimuli. These findings indicate that the dorsal AL is a site of auditory and somatosensory convergence and may therefore be a locus of convergence of conditioned and unconditioned stimuli in auditory fear conditioning.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Several lines of indirect evidence support the idea that this plasticity occurs as a result of a Hebbian mechanism through which depolarization of LA pyramidal neurons by the shock US coincident with weaker activation of the same cells by auditory CS inputs results in fear learning.
“Several lines of indirect evidence support the idea that this plasticity occurs as a result of a Hebbian mechanism through which depolarization of LA pyramidal neurons by the shock US coincident with weaker activation of the same cells by auditory CS inputs results in fear learning (8–18).”
From Optical activation of lateral amygdala pyramidal cells instructs associative fear learning (2010) · cites this paper as [13]
Cites
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292 · see citing works
Self-citationDifferential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.2.274 · Cited by 3,262 · see citing works
Self-citationModality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
Squire, L. R. (1984) · Springer eBooks · doi:10.1007/978-3-642-70094-1_32 · Cited by 2,126 · see citing works
The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction.
Aggleton, J. P. (1992) · Wiley-Liss eBooks · Cited by 1,536 · see citing works
The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning
LeDoux, J., Cicchetti, P., Xagoraris, A., & Romanski, L. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01062.1990 · Cited by 1,167 · see citing works
Self-citationThe Neurobiology of Learning and Memory
Thompson, R. F. (1986) · Science · doi:10.1126/science.3738519 · Cited by 1,159 · see citing works
Berendse, H. W., Graaf, Y. G.-D., & Groenewegen, H. J. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903160305 · Cited by 847 · see citing works
Conditioned Reflexes and Neuron Organization.
(1949) · Annals of Internal Medicine · doi:10.7326/0003-4819-31-6-1133_1 · Cited by 688 · see citing works
(1992) · Cited by 626 · see citing works
Topographic organization of neurons in the acoustic thalamus that project to the amygdala
LeDoux, J., Farb, C. R., & Ruggiero, D. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01043.1990 · Cited by 546 · see citing works
Self-citationLeDoux, J., Sakaguchi, A., & Reis, D. (1984) · The Journal of Neuroscience · doi:10.1523/jneurosci.04-03-00683.1984 · Cited by 532 · see citing works
Self-citationLeDoux, J. E., Ruggiero, D. A., & Reis, D. J. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902420204 · Cited by 530 · see citing works
Self-citationLearning and Computational Neuroscience: Foundations of Adaptive Networks
Gabriel, M., & Moore, J. (1990) · Cited by 519 · see citing works
Romanski, L. M., & LeDoux, J. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04501.1992 · Cited by 461 · see citing works
Self-citationThalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing
Turner, B. H., & Herkenham, M. (1991) · The Journal of comparative neurology · doi:10.1002/cne.903130208 · Cited by 437 · see citing works
Cellular neurophysiological approaches in the study of learning.
Kandel, E., & Spencer, W. A. (1968) · Physiological Reviews · doi:10.1152/physrev.1968.48.1.65 · Cited by 412 · see citing works
Romanski, L. M., & LeDoux, J. E. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.6.515 · Cited by 398 · see citing works
Self-citationMarburg, O. (2007) · Stereotactic and Functional Neurosurgery · doi:10.1159/000105833 · Cited by 387 · see citing works
Ledoux, J. E., Ruggiero, D. A., Forest, R., Stornetta, R., & Reis, D. J. (1987) · Journal of Comparative Neurology · doi:10.1002/cne.902640110 · Cited by 373 · see citing works
Self-citationPoggio, G. F., & Mountcastle, V. B. (1960) · PubMed · Cited by 306 · see citing works
Calford, M. B., & Aitkin, L. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-11-02365.1983 · Cited by 281 · see citing works
LeDoux, J. E., Farb, C. R., & Romanski, L. M. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90526-y · Cited by 261 · see citing works
Self-citationBordi, F., & LeDoux, J. E. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-07-02493.1992 · Cited by 218 · see citing works
Self-citationSananes, C. B., & Davis, M. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.1.72 · Cited by 216 · see citing works
Edeline, J., & Weinberger, N. M. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.1.81 · Cited by 214 · see citing works
Frysztak, R. J., & Neafsey, E. J. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.5.418 · Cited by 175 · see citing works
Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus
Wepsic, J. G. (1966) · Experimental Neurology · doi:10.1016/0014-4886(66)90053-7 · Cited by 171 · see citing works
Ryugo, D. K., & Weinberger, N. M. (1978) · Behavioral Biology · doi:10.1016/s0091-6773(78)92351-9 · Cited by 145 · see citing works
Information flow from sensation to emotion: Plasticity in the neural computation of stimulus value.
LeDoux, J. E. (1990) · Cited by 130 · see citing works
Self-citationRomanski, L. M., & LeDoux, J. E. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90379-l · Cited by 114 · see citing works
Self-citationStefanacci, L., Farb, C. R., Pitkänen, A., Go, G. ‐., LeDoux, J. E., & Amaral, D. G. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903230411 · Cited by 106 · see citing works
Self-citationInhibition in the medial geniculate body of the cat
Aitkin, L., & Dunlop, C. W. (1969) · Experimental Brain Research · doi:10.1007/bf00236108 · Cited by 89 · see citing works
Disterhoft, J. F., & Stuart, D. K. (1976) · Journal of Neurophysiology · doi:10.1152/jn.1976.39.2.266 · Cited by 89 · see citing works
Clugnet, M., LeDoux, J., & Morrison, S. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01055.1990 · Cited by 86 · see citing works
Self-citationGabriel, M., Miller, J. D., & Saltwick, S. E. (1976) · Physiological Psychology · doi:10.3758/bf03326563 · Cited by 82 · see citing works
Acoustic input to single neurons in pulvinar-posterior complex of cat thalamus
Phillips, D. P., & Irvine, D. R. F. (1979) · Journal of Neurophysiology · doi:10.1152/jn.1979.42.1.123 · Cited by 68 · see citing works
Supple, W. F., & Kapp, B. S. (1989) · Behavioral Neuroscience · doi:10.1037//0735-7044.103.6.1276 · Cited by 42 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
Self-citationCognitive neuroscience of emotional memory
LaBar, K. S., & Cabeza, R. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1825 · Cited by 1,834 · see citing works
The Emotional Brain, Fear, and the Amygdala
LeDoux, J. (2003) · Cellular and Molecular Neurobiology · doi:10.1023/a:1025048802629 · Cited by 1,818 · see citing works
Self-citationThe Amygdaloid Complex: Anatomy and Physiology
SAH, P., FABER, E. S. L., LOPEZ DE ARMENTIA, M., & POWER, J. (2003) · Physiological Reviews · doi:10.1152/physrev.00002.2003 · Cited by 1,745 · see citing works
Neuronal signalling of fear memory
Maren, S., & Quirk, G. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1535 · Cited by 1,428 · see citing works
Cortical pathways to the mammalian amygdala
McDonald, A. J. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00003-3 · Cited by 1,303 · see citing works
The neuroanatomical and neurochemical basis of conditioned fear
Fendt, M., & Fanselow, M. S. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00016-0 · Cited by 1,092 · see citing works
Molecular mechanisms of fear learning and memory
Johansen, J. P., Cain, C. K., Ostroff, L. E., & LeDoux, J. E. (2011) · Cell · doi:10.1016/j.cell.2011.10.009 · Cited by 1,012 · see citing works
Self-citationPitkänen, A., Savander, V., & LeDoux, J. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01125-9 · Cited by 980 · see citing works
Self-citationQuirk, G. J., Repa, J. C., & LeDoux, J. E. (1995) · Neuron · doi:10.1016/0896-6273(95)90092-6 · Cited by 808 · see citing works
Self-citationAmygdala Microcircuits Controlling Learned Fear
Duvarci, S., & Pare, D. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.042 · Cited by 751 · see citing works
The Neuroscience of Mammalian Associative Learning
Fanselow, M. S., & Poulos, A. M. (2005) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070213 · Cited by 683 · see citing works
A circuit mechanism for differentiating positive and negative associations
Namburi, P., Beyeler, A., Yorozu, S., Calhoon, G. G., Halbert, S. A., Wichmann, R., Holden, S. S., Mertens, K. L., Anahtar, M., Felix-Ortiz, A. C., et al. (2015) · Nature · doi:10.1038/nature14366 · Cited by 614 · see citing works
Olsson, A., & Phelps, E. A. (2007) · Nature Neuroscience · doi:10.1038/nn1968 · Cited by 622 · see citing works
Schafe, G. E., & LeDoux, J. E. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-18-j0003.2000 · Cited by 611 · see citing works
Self-citationSynaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning
Blair, H. T., Schafe, G. E., Bauer, E. P., Rodrigues, S. M., & LeDoux, J. E. (2001) · Learning & Memory · doi:10.1101/lm.30901 · Cited by 610 · see citing works
Self-citationMemory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective
Schafe, G. E., Nader, K., Blair, H. T., & LeDoux, J. E. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01969-x · Cited by 510 · see citing works
Self-citationEncoding of fear learning and memory in distributed neuronal circuits
Herry, C., & Johansen, J. P. (2014) · Nature Neuroscience · doi:10.1038/nn.3869 · Cited by 474 · see citing works
Goosens, K. A., & Maren, S. (2001) · Learning & Memory · doi:10.1101/lm.37601 · Cited by 451 · see citing works
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
Neural and cellular mechanisms of fear and extinction memory formation
Orsini, C. A., & Maren, S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.12.014 · Cited by 429 · see citing works
Auditory Processing across the Sleep-Wake Cycle
Portas, C. M., Krakow, K., Allen, P., Josephs, O., Armony, J. L., & Frith, C. D. (2000) · Neuron · doi:10.1016/s0896-6273(00)00169-0 · Cited by 392 · see citing works
The birth, death and resurrection of avoidance: a reconceptualization of a troubled paradigm
LeDoux, J. E., Moscarello, J., Sears, R., & Campese, V (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.166 · Cited by 348 · see citing works
Self-citationChapter 26 Emotional networks and motor control: a fearful view
(1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61880-4 · Cited by 364 · see citing works
Neural ensemble dynamics underlying a long-term associative memory
Grewe, B. F., Gründemann, J., Kitch, L. J., Lecoq, J. A., Parker, J. G., Marshall, J. D., Larkin, M. C., Jercog, P. E., Grenier, F., Li, J. Z., et al. (2017) · Nature · doi:10.1038/nature21682 · Cited by 351 · see citing works
Kulkarni, B., Bentley, D. E., Elliott, R., Youell, P., Watson, A., Derbyshire, S. W. G., Frackowiak, R. S. J., Friston, K. J., & Jones, A. K. P. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04098.x · Cited by 337 · see citing works
The role of the striatum in aversive learning and aversive prediction errors
Delgado, M. R., Li, J., Schiller, D., & Phelps, E. A. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0161 · Cited by 328 · see citing works
Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray
Johansen, J. P., Tarpley, J. W., LeDoux, J. E., & Blair, H. T. (2010) · Nature Neuroscience · doi:10.1038/nn.2594 · Cited by 312 · see citing works
Self-citationTsvetkov, E., Carlezon, W. A., Benes, F. M., Kandel, E. R., & Bolshakov, V. Y. (2002) · Neuron · doi:10.1016/s0896-6273(02)00645-1 · Cited by 321 · see citing works
Optical activation of lateral amygdala pyramidal cells instructs associative fear learning
Johansen, J. P., Hamanaka, H., Monfils, M. H., Behnia, R., Deisseroth, K., Blair, H. T., & LeDoux, J. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002418107 · Cited by 308 · see citing works
Self-citationSeeking a Spotless Mind: Extinction, Deconsolidation, and Erasure of Fear Memory
Maren, S. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.023 · Cited by 259 · see citing works
“For example, auditory and somatic stimuli excite LA neurons at short latencies (Johansen et al., 2010; Romanski et al., 1993), and fear conditioning greatly augments responses of LA neurons to auditory CSs (Goosens et al.”
BackgroundPetrovich, G. D., & Swanson, L. W. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01361-3 · Cited by 234 · see citing works
Amygdala microcircuits mediating fear expression and extinction
Pare, D., & Duvarci, S. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.02.014 · Cited by 193 · see citing works
Regulation of conditioned responses of basolateral amygdala neurons
GRACE, A., & ROSENKRANZ, J. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00909-5 · Cited by 172 · see citing works
Dendritic Spine Heterogeneity Determines Afferent-Specific Hebbian Plasticity in the Amygdala
Humeau, Y., Herry, C., Kemp, N., Shaban, H., Fourcaudot, E., Bissière, S., & Lüthi, A. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.019 · Cited by 148 · see citing works
Fanselow, M. S., Kim, J. J., Yipp, J., & De Oca, B. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.2.235 · Cited by 142 · see citing works
Pavlovian fear memory circuits and phenotype models of PTSD
Johnson, L. R., McGuire, J., Lazarus, R., & Palmer, A. A. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.07.004 · Cited by 140 · see citing works
Sah, P., Westbrook, R. F., & Lüthi, A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1417.020 · Cited by 138 · see citing works
Glover, E. M., Phifer, J. E., Crain, D. F., Norrholm, S. D., Davis, M., Bradley, B., Ressler, K. J., & Jovanovic, T. (2011) · Depression and Anxiety · doi:10.1002/da.20880 · Cited by 130 · see citing works
Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress
Salm, A. K., Pavelko, M., Krouse, E. M., Webster, W., Kraszpulski, M., & Birkle, D. L. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2003.11.005 · Cited by 125 · see citing works
Calandreau, L., Desmedt, A., Decorte, L., & Jaffard, R. (2005) · Learning & Memory · doi:10.1101/lm.92305 · Cited by 99 · see citing works
Linke, R. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00422.x · Cited by 88 · see citing works
Effects of repeated stress on excitatory drive of basal amygdala neurons in vivo
Padival, M., Quinette, D., & Rosenkranz, J. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.74 · Cited by 75 · see citing works
Exploring functions for the non-lemniscal auditory thalamus
Lee, C. C. (2015) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00069 · Cited by 63 · see citing works
McKinney, B. C., Sze, W., Lee, B., & Murphy, G. G. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.06.012 · Cited by 63 · see citing works
Current emotion research in behavioral neuroscience: the role(s) of the amygdala
Armony, J. L. (2013) · Emotion Review · doi:10.1177/1754073912457208 · Cited by 44 · see citing works
Serotonergic neuromodulation of synaptic plasticity
Higa, G. S. V., Viana, F. J. C., Francis-Oliveira, J., Cruvinel, E., Franchin, T. S., Marcourakis, T., Ulrich, H., & De Pasquale, R. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110036 · Cited by 29 · see citing works
- Authors
- Romanski, L. M., Clugnet, M.-C., Bordi, F., & LeDoux, J. E.
- Affiliations
- Yale University (US)
- New York University (US)
- Venue
- Behavioral Neuroscience
- Published
- 1993
- Volume
- 107
- Issue
- 3
- Pages
- 444-450
- ISSN
- 0735-7044 (ISSN-L)
- 1939-0084
- OpenAlex
- W2092568693
- Cited by
- 446
- References
- 38
- Citations by year
- 2026: 7 · 2025: 9 · 2024: 10 · 2023: 12 · 2022: 12 · 2021: 12 · 2020: 19 · 2019: 12 · 2018: 15 · 2017: 12 · 2016: 19 · 2015: 17 · 2014: 24 · 2013: 15 · 2012: 16
- FWCI
- 5.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioral Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH 46516, R01MH046516, MH38774)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- lateral amygdala, auditory fear conditioning, single-unit activity, footshock, acoustic stimuli
- MeSH terms
- Amygdala, Animals, Attention, Brain Mapping, Conditioning, Classical, Evoked Potentials, Auditory, Evoked Potentials, Somatosensory, Fear, Male, Neural Pathways, Neurons, Nociceptors, Rats, Sprague-Dawley, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
